Genetic basis for coordination of meiosis and sexual structure maturation in Cryptococcus neoformans

  1. Linxia Liu
  2. Guang-Jun He
  3. Lei Chen
  4. Jiao Zheng
  5. Yingying Chen
  6. Lan Shen
  7. Xiuyun Tian
  8. Erwei Li
  9. Ence Yang
  10. Guojian Liao
  11. Linqi Wang  Is a corresponding author
  1. Institute of Microbiology, Chinese Academy of Sciences, China
  2. Southwest University, China
  3. School of Basic Medical Sciences, Peking University Health Science Center, China

Abstract

In the human fungal pathogen Cryptococcus neoformans, sex can benefit its pathogenicity through production of meiospores, which are believed to offer both physical and meiosis-created lineage advantages for its infections. Cryptococcus sporulation occurs following two parallel events, meiosis and differentiation of the basidium, the characteristic sexual structure of the basidiomycetes. However, the circuit integrating these events to ensure subsequent sporulation is unclear. Here, we show the spatiotemporal coordination of meiosis and basidial maturation by visualizing event-specific molecules in developing basidia defined by a quantitative approach. Monitoring of gene induction timing together with genetic analysis reveals co-regulation of the coordinated events by a shared regulatory program. Two RRM family regulators, Csa1 and Csa2, are crucial components that specifically bridge meiosis and basidial maturation, further determining sporulation. We propose that the regulatory coordination of meiosis and basidial development serves as a determinant underlying the production of infectious meiospores in C. neoformans.

Data availability

The GEO accession number for the RNA-seq data reported in this study is GSE111975.

The following data sets were generated

Article and author information

Author details

  1. Linxia Liu

    State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Guang-Jun He

    State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Lei Chen

    State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Jiao Zheng

    College of Pharmaceutical Sciences, Southwest University, Chongqing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Yingying Chen

    State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Lan Shen

    State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Xiuyun Tian

    State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Erwei Li

    State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Ence Yang

    Department of Microbiology, School of Basic Medical Sciences, Peking University Health Science Center, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Guojian Liao

    Institute of Morden Biopharmaceuticals, School of Pharmaceutical Sciences, Southwest University, Chongqing, China
    Competing interests
    The authors declare that no competing interests exist.
  11. Linqi Wang

    State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    For correspondence
    wanglq@im.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5243-341X

Funding

Ministry of Science and Technology of the People's Republic of China (2018ZX10101004)

  • Linqi Wang

National Natural Science Foundation of China (31622004,31570138,31770163)

  • Linqi Wang

Chinese Academy of Sciences Key Project (QYZDB-SSW-SSMC040)

  • Linqi Wang

National Natural Science Foundation of China (31501008)

  • Guang-Jun He

National Natural Science Foundation of China (31501009)

  • Xiuyun Tian

The funders had roles in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Joseph Heitman, Duke University, United States

Version history

  1. Received: May 26, 2018
  2. Accepted: October 2, 2018
  3. Accepted Manuscript published: October 3, 2018 (version 1)
  4. Version of Record published: November 14, 2018 (version 2)

Copyright

© 2018, Liu et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Linxia Liu
  2. Guang-Jun He
  3. Lei Chen
  4. Jiao Zheng
  5. Yingying Chen
  6. Lan Shen
  7. Xiuyun Tian
  8. Erwei Li
  9. Ence Yang
  10. Guojian Liao
  11. Linqi Wang
(2018)
Genetic basis for coordination of meiosis and sexual structure maturation in Cryptococcus neoformans
eLife 7:e38683.
https://doi.org/10.7554/eLife.38683

Share this article

https://doi.org/10.7554/eLife.38683

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